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Underwater Domains in Yellowstone Lake Hydrothermal Vent Geochemistry and Bacterial Chemosynthesis

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Underwater Domains in Yellowstone Lake Hydrothermal Vent Geochemistry and Bacterial Chemosynthesis Russell L. Cuhel, Carmen Aguilar, Patrick D. Anderson, James S. Maki, Robert W. Paddock, Charles C. Remsen, J. Val Klump, and David Lovalvo Abstract Reduced inorganic compounds of geothermal-origin hydrogen sulfide (H2S), iron (Fe[II]), and methane (CH4) were common but not ubiquitous components of hydrothermal vent fluids of Yellowstone Lake at concentrations capable of supporting chemolithoautotrophic (geochemical-oxidizing, carbon dioxide (CO2)-fixing) bacterial growth. Closely linked to the presence of reduced geo- chemicals was abundance of chemosynthetic bacteria and dark CO2 fixation activity. Pronounced productivity at vent sites in the northern basin (Mary and Sedge Bays, Storm and Steamboat Points, and east of Stevenson Island) was accompanied by reduced sulfur stimulation in near-vent receiving waters, while none of these characteristics were found in West Thumb vent fields. Per-liter bac- terial productivity at vents (to 9.1 µgC/L/hour) could reach algal photosynthesis in surface waters (to 8.9 µgC/L/hour). Thermophilic (heat-loving) sulfur- and methane-oxidizing bacteria were isolated from vent orifice waters, and CO2 fix- ation incubations at 50°C indicated that the majority of chemosynthesis within the vents themselves was optimal at high temperatures. Receiving waters had much less activity at 50°C than at ambient temperature (4–20°C), distinguishing populations of mesophilic (moderate-temperature) bacteria that had also responded to the input of geochemicals from vents. Strong evidence for mineral- dependent bacterial productivity was obtained, with limited data suggesting an influence of lake stage or outflow on vent and productivity characteristics. Introduction For decades the colorful mats of bacteria and algae surrounding bubbling vents and fumaroles at Yellowstone National Park have been a focus of both touristic and scientific interest. It is with no small wonder that people look upon the growth of microorganisms in the often very hot, very corrosive fluids. Yet the interaction of biology with geothermal and geochemical energy may be more ancient than any other ecology. Prior to the mid-1970s, many scientists favored the theory of organic matter formation in the atmosphere and initial biological activity in surface brine pools using lightning energy as the primary catalyst (c.f. Miller 1953; Oro et al. 1990). Following the discovery of deep-sea hydrothermal geoecosystems in the mid-1970s, an additional hypothesis was developed, invok- ing organic matter formation and biological assembly in the high-temperature (to Yellowstone Lake 27 Cuhel, Aguilar, Anderson, Maki, Paddock, Remsen, Klump, and Lovalvo 350°C), high-pressure (>200 atm) deep-sea vents and surroundings. Both theo- retical and experimental evidence supporting each theory exist, and in fact the two concepts are not mutually exclusive. Early life certainly was microbial, at least tolerant of high temperatures, and predominantly made use of chemical energy for metabolic needs. At present, the highest temperatures for growth range to 113°C (Stetter 1999) and the isolated organisms are involved in methane and sulfur transformations. Yellowstone National Park offers a variety of habitats from hot (but <96°C), dissolved geo- chemical-laden (often to saturation with silicate or carbonate) surface springs and geysers with high microbial diversity (Barns et al. 1994) to hotter (to 130°C), dissolved geochemical-rich (but not saturated) waters and gases of Yellowstone Lake underwater vents and fumaroles. From a biogeochemical and ecological point of view, Yellowstone Lake is appealing because observed maximum vent- fluid temperatures range around or just above the limits for microbial life (Huber et al. 1989; Jørgensen et al. 1992), yet many of the same physical and geochem- ical characteristics of marine vents are preserved. Other freshwater hydrothermal sites have been identified, including massive sulfide deposits in Lake Tanganyika, East Africa (Tiercelin et al. 1989, 1993); hot-water vents in Lake Baikal, Russia (Crane et al. 1991; Shanks and Callender 1992), and deep micro- bial mats in Crater Lake, Oregon, USA (Dymond et al. 1989). Given the geo- chemically derived source of nutrition and the typically harsh physicochemical habitats in which they thrive, it is understandable that the bacteria known as lithotrophs (literally “rock eaters”) are usually the dominant forms of life in such environments. While they provide further rationale for the study of freshwater systems, few are as tractable as Yellowstone Lake for accessibility to study. The Yellowstone caldera underlies the northern half of Yellowstone Lake, while the Yellowstone River inflow and the southern half of the lake lie outside the caldera boundary.Within the caldera, geothermally heated subsurface water percolating through hot rocks above the magma chamber becomes enriched in carbonate, silicate, and chloride, with some locations additionally rich in methane, iron and sulfide. The park is world-renowned for its geothermal activ- ity. This provides a significant opportunity to delineate vent geochemical effects on bulk lake water composition, because enrichment occurs far from the most significant surface inflow, which is the Yellowstone River in the Southeast Arm (Figure 1). The northern half of Yellowstone Lake is strongly influenced by underwater geothermal hot springs and gas fumaroles. These features release water with high concentrations of silicate and bicarbonate as well as reduced materials of mineral origin, including hydrogen sulfide, Fe[II], methane, and, more rarely, ammonia into the bottom waters. While the vents of Yellowstone Lake resemble deep-sea hydrothermal systems in some important respects, the nearly closed nature of the basin and the relatively small volume of receiving waters provides additional opportunities for process research. Because riverine inputs and outputs may be estimated, Yellowstone Lake geothermal and biogeo- chemical activities are amenable to budgeting by mass balance (inputs + change = outputs). 28 6th Biennial Scientific Conference Underwater Domains Figure 1. Map of Yellowstone Lake showing areas of underwater hydrothermal features sampled by ROV. West Thumb samples ring the entire basin, and Mary Bay, Sedge Bay, Steamboat Point, and Storm Point samples were also within 300 m of shore. Stevenson Island collections were made in the deep canyons just east of the island. Southeast Arm samples were taken midway down the arm (65–90 m water depth). Yellowstone River inlet samples were taken by NPS personnel well upstream of the mouth. Work over the last 10 years on the development of remotely operated vehicle (ROV) survey and sampling technology (Marocchi et al. 2001; Remsen et al., this volume) demonstrated the absolute necessity of remote sampling of the deep, hot, seemingly inhospitable fluids of Yellowstone Lake vents. Starting with a simple Mini-Rover system consisting of video and still cameras and a claw with small pump-driven sipper tube, photographic surveys and water samples suitable - = + for limited dissolved geochemical (Cl , SiO2, SO4 , Na , etc.) and dissolved gas 222 (CH4, CO2, Rn) analysis were obtained (Klump et al. 1988). Combining the submersible results with surface-collected samples from the inlet at Southeast Yellowstone Lake 29 Cuhel, Aguilar, Anderson, Maki, Paddock, Remsen, Klump, and Lovalvo Arm and the outlet at Fishing Bridge, it became apparent that aqueous species and gases found in vent fluids were also significantly enriched in lake water rel- ative to surface inflows (Table 1) and in some cases comparable to marine vent- Table 1. Mineral content of mid-Atlantic Ridge seawater and marine vents compared with Yellowstone Lake inflow, outflow, and freshwater vents, 1994–1998 sampling results. ing systems. Although near-surface groundwater may contribute to enrichment, exceptionally strong signals from such geochemical indicators as radon-222 (derived from deep-rock degassing) and high flux rates of methane across the air–water interface imply a major role for submarine vents and fumaroles. Visual evidence of a long history of submarine geothermal activity is abun- dant in West Thumb, Mary Bay, Sedge Bay, Steamboat Point, and even in the very deep waters (120 m) off Stevenson Island, all within the caldera boundary (Marocchi et al. 2001). “Vent hole with white ppt. (323'); large relic pipe (176'); sponge attached to relic structure (176'); sulfide seeps, white ppt. (106'); bacter- ial mat on relic (110'); hot water vent with leeches (143'); sulfide fumaroles with white ppt. (143'); shimmering water with zooplankton swarm (310'); fish near hot water vent (128'); probe in 120°C hot vent—black smoker! (131')” are a few of the annotations from still and video images catalogued from the last few years (Remsen et al., this volume). Submersible observations reveal some significant similarities and some major differences between the freshwater Yellowstone Lake hydrothermal systems and marine deep-sea hydrothermal vents (Humphris et al. 1995). Both show power- ful, highly localized geochemical process signals in solid-phase deposits and dis- 30 6th Biennial Scientific Conference Underwater Domains solved chemical species. Both demonstrate finite lifetimes through existence of relic vent fields. Both act as focal points for biological activity (Page et al. 1991; Toulmond et al. 1994; Nelson et al. 1995), particularly in the
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